Bull. Natl. Mus. Nat. Sci., Ser. B, 39(1), pp. 11–14, February 22, 2013

Opegrapha phaeophysciae (, ), a Lichenicolous Ascomycete, New to Japan

Andreas Frisch* and Yoshihito Ohmura

Department of Botany, National Museum of Nature and Science, Amakubo 4–1–1, Tsukuba, Ibaraki 305–0005, Japan * E-mail: [email protected]

(Received 16 November 2012; accepted 19 December 2012)

Abstract phaeophysciae is newly reported for Japan from Hokkaido and central Honshu, and a detailed description of the species is provided based on the Japanese collections. This species has previously been found on Phaeophyscia hispidula and was known only from Far East Russia. In Japan, O. phaeophysciae was found on the thallus of P. limbata, a species closely related to P. hispidula.

Key words : , parasite, , Phaeophyscia hispidula, Phaeophyscia limbata.

Lichenicolous fungi comprise a large and tax- Materials and Methods onomically diverse group of about 1,800 species growing as obligate parasites or saprotrophs on Anatomical examinations were made using (Lawrey and Diederich, 2003, 2011). hand-cut sections mounted in water and Lactic They mainly belong to the , and Cotton Blue. Chemical reactions of the ascomata some of them (less than 5%) belong to Basidio- were investigated in 1% aqueous iodine solution mycota (Lawrey and Diederich, 2003). Licheni- (I), 0.25% aqueous iodine solution (Idil), 1% colous fungi have not been well studied in Japan, aqueous iodine solution after pretreatment with and only 21 species have been reported (Kuro- 10% aqueous potassium hydroxide solution (KI), kawa and Kashiwadani, 2006), of which 10 spe- 10% aqueous potassium hydroxide solution (K), cies alone belong to the calicioid genera Chaeno- and 10% nitric acid (N). Due to the absence of a thecopsis and Sphinctrina (Tibell and Thor, sufficient number of well-developed spores in the 2003) and other species belong to various phylo- Japanese specimens, spore measurements are genetic groups, i.e. Cornutispora, Distopyrenis, given as min.-max. values only. Leptosphaeria, , Phacopsis, Rhab- All specimens examined are housed in TNS dospora, and Stigmidium. except otherwise indicated. In the present contribution, we newly report on Opegrapha phaeophysciae that has recently been Results and Discussion collected from the thallus of Phaeophyscia lim- bata on Hokkaido and was subsequently discov- Opegrapha phaeophysciae R. Sant., Diederich, ered on five additional specimens of that species Ertz & Christnach, Biblioth. Lichenol. 91: 132 from Hokkaido and central Honshu preserved in (2005). the National Museum of Nature and Science [Fig. 1] (TNS). Type: RUSSIA, Primorskii Region. Lazovskii District, Lazovskii Reserve, small hill along the seashore, ca. 5 km S of Glazovska village, 12 Andreas Frisch and Yoshihito Ohmura

Fig. 1. Opegrapha phaeophysciae (Frisch 12/Jp183, TNS). A. Growth habit on Phaeophyscia limbata. B. Group of ascomata (the small picture shows a horizontal section through an ascoma with marginally divided hyme- nium). Scale bars: A=1.0 mm, B=0.5 mm. Opegrapha phaeophysciae, a Lichenicolous Ascomycete, New to Japan 13

41°01′N, 134°10′E, 30 m alt., on Quercus manshu- 750 m alt. It was found on Phaeophyscia limbata rica in the southern slope towards the sea, on growing on various deciduous trees, including Phaeophyscia hispidula (thallus), 22 ix 1991, R. Ulmus davidiana var. japonica, Acer miyabei, Santesson 33270 (=R. Santesson, Fungi and Zelkova serrata. Previously, O. phaeophys- lichenicoli exsiccati no. 360) (UPS holotype, not cia was only known from the Primorskii Region seen; TNS isotype!). of eastern Russia, where it was collected from ASCOMATA solitary, scattered to crowded on the thallus of Phaeophyscia hispidula (Ertz et al., the upper side of the host thallus, immersed first 2005). Phaeophyscia hispidula and P. limbata but soon emergent, black, rounded, slightly con- are closely related to each other (Kashiwadani, vex to flattened, basally not constricted, 0.2– 1984) and could be treated at subspecies level 0.6 mm diam., with fragments of the host cortex within a common taxon (Poelt, 1974). attached to the younger stages; upper stromatic NOTES. The Japanese specimens agree well layer irregularly reticulate-fissured and/or with a with the isotype of O. phaeophysciae (R. Santes- ring-fissure along the outer margin, occasionally son, Fungi Lichenicoli Exsiccati no. 360) in breaking away in the center to expose the hyme- TNS. By checking about 300 Japanese collec- nium. STROMA dark brown, 90–160 µm tall, in tions of Phaeophyscia hispidula and P. limbata K olivaceous brown, in N more orange brown, preserved in TNS, only five additional specimens pigment Atra-brown; hymenium in horizontal of O. phaeophysciae were found. The species is section undulate to marginally divided and often possibly rare in Japan, but selective collection of with one to three rounded columns of stromatic ‘clean’ specimens in the field (i.e., lichen speci- plectenchyma, in transversal section with one to men without parasite fungi on the thallus) might three subspherical to extensive loci; marginal and also cause the lack of O. phaeophysciae in the apical stromatic layer 20–40 µm thick, some- collections. times missing in the central portions of the asco- Opegrapha phaeophysciae is the third para- mata. SUBHYMENIUM hyaline, Idil+ pale blu- sitic Opegrapha species known to Japan besides ish, I+ pale red mottled with pale blue, KI+ O. lichenicola growing on foliicolous crustose blue, 10–15 µm tall. HYMENIUM hyaline, Idil+ lichens [e.g., Eremothecella macrosperma, Mazo- pale red, I+ red, KI+ blue, 60–100 µm tall. sia melanophthalma, and problably Porina sp.]

EPIHYMENIUM brownish, Idil+, I+ and KI+ (Thor et al., 2000) and O. foreaui [=O. trassii blue, 15–20 µm tall. PARAPHYSOIDS abun- (see Hafellner, 2002)] on Heterodermia sp. (Cop- dant, branched and anastomosing, 2–2.5 µm pins and Kondratyuk, 1998). thick, apically slightly swollen. ASCI Opegra- The supraspecific of the about 58 pha-type, clavate, with an apical K/I+ blue parasitic Opegrapha species (Lawrey and Died- ring structure, 4–spored, 50–85×12–16 µm. erich, 2011) is not resolved at present, but most ASCOSPORES hyaline, becoming brown and species are expected not to belong to Opegrapha granular warty at maturity, elongate ellipsoid, s. str. (Ertz et al., 2005). Opegrapha phaeophys- (4–)6 septate, slightly constricted at the septa, ciae is placed in the parasitic O. anomea-group, 21–28(–32)×4.0–6.0 µm, the median cell often which differs from Opegrapha (s. str.) mainly by somewhat elongated. PERISPORE ca. 1 µm the stromatic uni- to poorly multilocular roundish thick, with a brown granulose pigmentation ascomata (Ertz et al., 2005). The species in this located on the outer wall at maturity. PYCNIDIA group show affinities to the not observed. Fée and the phylogenetic relationship towards ECOLOGY AND DISTRIBUTION. In this genus needs further study (Ertz et al., 2004, Japan, O. phaeophysciae is known from three 2005). localities on Hokkaido and the mountains of cen- The Japanese common name for this species is tral Honshu at altitudes from sea-level up to given here as “Yadori-kigô-goke”. 14 Andreas Frisch and Yoshihito Ohmura

Specimens examined. JAPAN. Hokkaido. lichenicolous Opegrapha species (, Asco- Prov. Abashiri: Yobito, Abashiri-city, over Phaeo- mycota) with 3-septate ascospores on Pertusaria and physcia limbata on the bark of an unidentified Ochrolechia. Botanical Journal of the Linnean Society 144: 235–241. tree in shady deciduous forest at the shore of Ertz, D., Christnach, C., Wedin, M. and Diederich, P. Abashiri Lake, 43°59′36.0″N, 144°12′18.7″E, 2005. A world monograph of the genus Plectocarpon 25 m, 29 v 2012, A. Frisch 12/Jp183 & Y. Oh- (Roccellaceae, ). Bibliotheca Lichenologica mura (TNS, UPS, hb Frisch). Prov. Ishikari: 91: 3–155. Maruyama, Sapporo-city, on bark of Ulmus Hafellner, J. 2002. Bemerkenswerte Funde von Flechten und lichenicolen Pilzen auf makaronesischen Inseln VI. davidiana var. japonica, ca. 20 m, 23 vii 1970, H. Über einige Neufunde. Fritschiana 36: 11–17. Kashiwadani 7500, 7502 (TNS); ibid., on bark of Kashiwadani, H. 1984. On two species of Phaeophyscia Acer miyabei, ca. 200 m, 23 vii 1970, H. Kashiwa- in Japan. Bulletin of the National Science Museum, dani 7497 (TNS). Honshu. Prov. Shinano: Series B 10: 127–132. Hiraide, Shiojiri-city, on bark of Zelkova serrata, Kurokawa, S. and Kashiwadani, H. 2006. Checklist of Japanese lichens and allied fungi. National Science ca. 750 m, 28 x 1986, H. Kashiwadani 23660, Museum Monographs 33: 1–157. 23662 (TNS). Lawrey, J. D. and Diederich, P. 2003. Lichenicolous fungi: interactions, evolution, and biodiversity. The Bryologist 106: 81–120. Acknowledgments Lawrey, J. D. and Diederich P. 2011. Lichenicolous fungi This study is partly funded by the Grant-in- – worldwide checklist, including isolated cultures and sequences available (http://www.lichenicolous.net Aid relating to JSPS Postdoctoral Fellowship for [12/21/2012]). Foreign Researchers (no. 23–01706), which is Poelt, J. 1974. Die Gattungen Physcia, Physciopsis und gratefully acknowledged. Physconia (lichenes, ), Flechten des Hima- laya 6. Khumbu Himal 6: 57–99. Thor, G., Lücking, R. and Matsumoto, T. 2000. The foli- References icolous lichens of Japan. Symbolae Botanicae Upsa- Coppins, B. J. and Kondratyuk, S. Y. 1998. Opegrapha lienses 32(3): 1–72. trassii sp. nov., a new lichenicolous fungus on Hetero- Tibell, L. and Thor, G. 2003. Calicioid lichens and fungi dermia. Folia Cryptogamica Estonica 32: 9–14. of Japan. Journal of the Hattori Botanical Laboratory Ertz, D., Diederich, P. and Miadlikowska, J. 2004. The 94: 205–259.